Status, trends and management of sturgeon and paddlefish fisheries

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1 F I S H and F I S H E R I E S, 2005, 6, Status, trends and management of sturgeon and paddlefish fisheries Ellen K Pikitch 1,2 *, Phaedra Doukakis 1,2 *, Liz Lauck 3, Prosanta Chakrabarty 4 & Daniel L Erickson 3 1 Pew Institute for Ocean Science, 126 East 56th Street, Mezzanine, New York, NY 10022; 2 University of Miami, Rosenstiel School of Marine and Atmospheric Science, 4600 Rickenbacker Causeway, Key Biscayne, FL ; 3 Marine Conservation Program, Wildlife Conservation Society, 2300 Southern Blvd., Bronx, NY 10460; 4 Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA Abstract The 27 extant species of sturgeons and paddlefishes (Order Acipenseriformes) represent a unique and relict lineage of fishes. Producers of coveted black caviar, sturgeons are one of the most valuable wildlife commodities on earth. The group is among the most endangered fishes with all species listed under Convention on International Trade in Endangered Species (CITES) Appendix I (two species) or II (25 species), only two species considered Lower Risk by IUCN, four of the nine US taxa and one Caspian species protected under the Endangered Species Act, and local extinctions recorded for 19 of 27 species. Despite their well-publicized imperilled status, commercial pressure on 15 species persists. Here, after reviewing the biological characteristics of sturgeons and paddlefishes and their commercial use, an overview of global fisheries is presented. The synopsis demonstrates that, with few exceptions, sturgeon and paddlefish are imperilled across the globe and long-term survival in the wild is in jeopardy. All major sturgeon fisheries have surpassed peak productivity levels, with 70% of major fisheries posting recent harvests <15% of historic peak catches and 35% of the fisheries examined crashing within 7 20 years of inception. Even in Caspian Sea fisheries, the most important globally, present catches are below 10% of historic peak landings. Improved domestic and international fisheries management and attention to habitat and species restoration is now needed. Although captive rearing offers promise for caviar alternatives and endangered species restoration, it must advance cautiously to avoid environmental harm. To ensure a continued supply of caviar and the survival of these unique fishes we offer recommendations for priority conservation action for the future. Correspondence: Phaedra Doukakis, Pew Institute for Ocean Science, 126 East 56th Street, Mezzanine, New York, NY 10022, USA Tel.: Fax: pdoukakis@ rsmas.miami.edu *These authors contributed equally to this work. Received 15 July 2004 Accepted 26 July 2005 Keywords Acipenseriformes, aquaculture, caviar, conservation, Convention on International Trade in Endangered Species Introduction 234 Overview of Acipenseriformes 234 International harvest and trade 240 Major global fisheries 241 Caspian Sea 241 Black Sea and Sea of Azov 245 Ó 2005 Blackwell Publishing Ltd 233

2 Amur River basin 247 Siberian rivers 248 Western North America 248 Anadromous species in eastern North America 249 Potamodromous species in inland and eastern North America 250 Sturgeon fisheries of the world: observations and recommendations 251 Status of Acipensiformes populations and fisheries 251 Recommendations on conservation priorities 253 Acknowledgements 257 References 257 Introduction Twenty-seven extant species of sturgeons and paddlefishes (Order Acipenseriformes) inhabit the rivers, estuaries, near-shore oceanic environments and inland seas of the northern hemisphere (Table 1; Fig. 1; Birstein 1993; Grande and Bemis 1996; Bemis et al. 1997; Bemis and Kynard 1997). A unique and relict lineage important in the evolutionary history of fishes, many sturgeons and paddlefishes now face extinction because of overfishing, pollution and habitat degradation (Birstein 1993). Producers of black caviar, the unfertilized eggs of true sturgeon, and commercial roe, the unfertilized eggs of paddlefish, the group has experienced decades of intense exploitation fuelled by a lucrative international caviar market. Their fisheries have undergone boom and bust cycles, with overexploitation resulting in harvest and population declines. Few viable sturgeon fisheries now remain. Recent published works offer summaries of Acipenseriformes aquaculture, biology, conservation, evolution and genetics (Birstein 1993; Dettlaff et al. 1993; Bemis et al. 1997; Bemis and Kynard 1997; Birstein et al. 1997a,c; Findeis 1997; Choudhury and Dick 1998; Billard and Lecointre 2001; Chebanov and Billard 2001; Fontana et al. 2001; Mims 2001; Van Winkle et al. 2002). After briefly reviewing these topics, we review the status and management of 14 commercially important species, focusing on species for which improvements in fisheries management are most critical to restoration and recovery. Species threatened exclusively by habitat degradation, too endangered to support commercial fishing or fully protected from exploitation are only briefly mentioned. Overview of Acipenseriformes Part of the Gnathostomata or jawed fishes, sturgeons and paddlefishes represent an ancient Actinopterygian lineage. Dating from the Lower Jurassic (200 Myr BP), these living fossils retain primitive characters including a heterocercal caudal fin and ganoid scales (Gardiner 1984). Characters such as a cartilaginous endoskeleton and hyostylic jaw suspension led to early classification as sharks (Bemis et al. 1997). Since their genesis in the Tethys Sea, Acipenseriformes lineages diverged in Europe and Asia and later radiated in North America (Bemis and Kynard 1997; Birstein et al. 1997b). All extant and fossil sturgeons and paddlefishes are from the temperate northern hemisphere with a distribution closely tied to the former Laurasian landmasses (Eurasia, North America) (Grande and Bemis 1996; Bemis et al. 1997). Some of the largest rivers and inland waterbodies are important sturgeon and paddlefish habitats (Table 1; Fig. 1). The Order Acipenseriformes is divided into two families, Acipenseridae (sturgeon) and Polyodontidae (paddlefish) (Table 1; Berg 1940; Grande and Bemis 1996; Bemis et al. 1997). The 25 extant species of sturgeon have spindle-shaped bodies covered by five rows of bony scutes and snouts with sensory barbells. The two extant species of paddlefish lack scales and scutes and have a large extended rostrum. Some taxonomic designations based upon morphology have been challenged by molecular studies and the true number of species and subspecies remains contentious (Grande and Bemis 1996; Mayden and Kuhajda 1996; Bemis et al. 1997; Birstein and Bemis 1997; Birstein et al. 1997b, 2002; Findeis 1997; Birstein and DeSalle 234 Ó 2005 Blackwell Publishing Ltd, FISH and FISHER IES, 6,

3 Table 1 Species of Acipenseriformes, current geographical range and conservation status. General references include Birstein 1993; Bemis and Kynard 1997; Birstein et al. 1997a; CITES 2000; Billard and Lecointre 2001; Williamson Binomials Common name Geographical range Status 2 Range contractions A. baerii (Brandt, 1869) 3 coast (US ESA); SC Siberian sturgeon Siberian rivers VU (IUCN); App. II 1 Some Yenisey and Lena river reaches A. baerii baerii Siberian sturgeon Ob R. basin EN (IUCN) A. baerii baicalensis Baikal sturgeon Lake Baikal, Siberia VU (IUCN) A. baerii stenorrhynchus Lena River sturgeon Eastern Siberian rivers EN (IUCN) A. brevirostrum Shortnose sturgeon North America, eastern VU (IUCN); App. I; E (Lesueur, 1818) 4 (COSEWIC); EN (CT, FL, GA, MD, MA, NH, NJ, NY, NC, PA, SC, VA) A. dabryanus (Duméril, 1869) 5 Yangtze/Dabry s sturgeon Yangtze River system CR (IUCN); App. II Lower Yangtze River A. fulvescens (Rafinesque, 1817) 6 Canada; Hudson-James Bay, Lake sturgeon Great Lakes, lakes of south Mississippi River drainage A. gueldenstaedtii (Brandt, 1833) VU (IUCN); App. II; SC (GA, NC), EN (IL, IN, IA, MO, OH, PA, TN, VT), TH (MI, NE, NY) EX (AL, AR, MS, WV), Mississippi Delta; Lakes Winnipeg, Ontario and Erie Russian sturgeon Ponto-Caspian region EN (IUCN 1 ); App. II 1 Upper Danube, Volga, Kuban rivers A. g. gueldenstaedtii Caspian Sea A. g. colchicus Black Sea A. g. colchicus Azov Sea A. medirostris (Ayres, 1854) 7 Green sturgeon North America, Pacific coast VU (IUCN); App. II; SC (COSEWIC); SC (California) A. mikadoi (Hilgendorf, 1892) 8 Sakhalin sturgeon Pacific Ocean, Amur R. to N. Japan, Bering Sea, Tumnin R. EN (IUCN); App. II Korea Southern population segment: Upper Columbia A. naccarii (Bonaparte, 1836) 9 Adriatic sturgeon Adriatic Sea, Po R. VU (IUCN); App. II Range contraction likely A. nudiventris EX (Aral Sea, upper Danube R.) (Lovetsky, 1828) 10 and rivers Ship sturgeon Caspian, Black and Aral seas A. oxyrinchus 11 (Mitchill, 1814) Atlantic sturgeon Gulf of Mexico and northern S. America A. oxyrinchus desotoi Gulf sturgeon N. America, east coast, Florida A. oxyrinchus oxyrinchus Atlantic sturgeon to Labrador EN (IUCN; Black, Caspian), CR (IUCN; Danube River), App. II LR (IUCN); App. II 1 A. persicus (Borodin, 1897) Persian sturgeon Ponto-Caspian EN (IUCN); App. II 1 A. persicus persicus Caspian Sea VU (IUCN) A. persicus colchicus Black Sea and rivers EN (IUCN) A. ruthenus (Linnaeus, 1758) Sterlet Caspian and Black seas and watershed; Siberian rivers VU (IUCN); T (US ESA); TH (AL, LA); SC (FL, GA); EN (MS) LR (IUCN); TH (CT, PA); EN (DE, MA); SC (FL, NC, VA); VU (IUCN); App. II Ó 2005 Blackwell Publishing Ltd, F I S H and F I S H E R I E S, 6,

4 Table 1 Continued. Binomials Common name Geographical range Status 1 Range contractions A. schrenckii (Brandt, 1869) 12 Amur River sturgeon Amur R. system EN (IUCN); App. II A. sinensis (Gray, 1835) 13 Chinese sturgeon Yangtze R. system EN (IUCN); App. II Upper Yangtze A. stellatus (Pallas, 1771) Stellate sturgeon Ponto-Caspian EN (IUCN); App. II 1 Upper Danube, Volga, Kuban rivers A. s. stellatus Caspian Sea VU (IUCN) A. s. ponticus Black Sea EN (IUCN) A. s. donensis Sea of Azov EN (IUCN) A. sturio (Linnaeus, 1758) 14 Atlantic (Baltic) sturgeon Baltic, Eastern N. Atlantic, Mediterranean, Black Sea A. transmontanus White sturgeon North America, west coast, (Richardson, 1836) 15 Gulf of Alaska to Baja CR (IUCN); App. I Throughout Europe LR (IUCN); EN (IUCN; Kootenai R. population); E (US ESA, Kootenai R. population); E (COSEWIC); IM (British Columbia) Huso dauricus (Georgi, 1775) Kaluga sturgeon Amur R. system EN (IUCN); App. II H. huso (Linnaeus, 1758) Ponto-Caspian EN (IUCN); T (US ESA); App. II 1 Upper Danube, Dnieper, Volga, Kuban rivers; EX EX (IUCN) H. h. caspicus Caspian Sea EN (IUCN) H. h. ponticus Black Sea EN (IUCN) H. h. maeoticus Sea of Azov Adriatic Sea CR (IUCN) Pseudoscaphirhynchus CR (IUCN); App. II Possibly extinct fedtschenkoi (Kessler, 1872) 16 Central Asia) Syr-Dar shovelnose sturgeon Syr-Darya R. (Kazakhstan, P. hermanni (Kessler, 1877) 17 Small Amu Dar shovelnose sturgeon P. kaufmanni (Kessler ex. (Bogdanov), 1874) 18 Large Amu-Dar shovelnose sturgeon Amu-Darya R. (Uzbekistan, Central Asia) Amu-Darya R. (Turkmenistan, Uzbekistan and Tajikistan, Central Asia) CR (IUCN); App. II EN (IUCN); App. II Upper Amu Darya R. Scaphirhynchus albus (Forbes and Pallid sturgeon Missouri Mississippi R. basins EN (IUCN); App. II E (USA ESA); EN Richardson, 1905) 19 (US 1 ) S. platorynchus (Rafinesque, 1820) 20 Grande (TX)) Shovelnose sturgeon Missouri Mississippi R. basins VU (IUCN); App. II; EN (OH); TH (TX) EX (Al? NM, NC, PA, WV?; Rio S. suttkusi (Williams and Clemmer, 85% of former range 1991) 21 (AL); EN (MS) Alabama sturgeon Missouri- Mississippi R. basins CR (IUCN); App. II; E (USA ESA); PR 236 Ó 2005 Blackwell Publishing Ltd, FISH and FISHER IES, 6,

5 Table 1 Continued. Binomials Common name Geographical range Status 1 Range contractions Polyodon spathula North American paddlefish Mississippi R. system VU (IUCN); App. II; E (COSEWIC); TH (MI, (Walbaum in Artedi, 1792) 22 OH, TX, WI), SC (T), EN (NC, VA) EX (Ontario, MD, NC, NY, PA) Psephurus gladius Chinese paddlefish Yangtze R. CR (IUCN); App. II; East China Sea, Yellow River, some (Martens, 1862) 23 Yangtze River tributaries 1 All populations included in designation. 2 IUCN Listings: VU, vulnerable; LR, lower risk; CR, critically endangered; EX, extinct. USA Endangered Species Act Listing: E, endangered; T, threatened. CITES Listings: App. I, Appendix I; App. II, Appendix II. Canada Listing (COSEWIC): SC, special concern; E, Extirpated. State and province classifications: TH, threatened; EN, endangered; EX, extinct; IM, imperilled; SC, special concern; PR, protected non-game species. State Abbreviations for US listings as follows: Alabama, AL; Arkansas, AR; CT, Connecticut; DE, Delaware; FL, Florida; GA, Georgia; ID, Idaho; IL, Illinois; IN, Indiana; IA, Iowa; KS, Kansas; KY, Kentucky; LA, Louisiana; MA, Massachusetts; MD, Maryland; MI, Michigan; MN, Minnesota; MS, Mississippi; MO, Missouri; MT, Montana; NE, Nebraska; NJ, New Jersey; NM, New Mexico; NY, New York; NC, North Carolina; ND, North Dakota; OH, Ohio; OK, Oklahoma; PA, Pennsylvania; SC, South Carolina; SD, South Dakota; TN, Tennessee; TX, Texas; VT, Vermont; VA, Virginia; WI, Wisconsin; WY, Wyoming. Sources: Birstein et al. 1997a; Williamson Solovov and Vasila v (1989); Ruban (1997). 4 Kynard (1997); NMFS (1998a); Grunwald et al. (2002); Kynard and Horgan (2002). 5 Wei et al. (1997, 2004); Zhuang et al. (1997). 6 Ferguson and Duckworth (1997); Thuemler (1997); Knights et al. (2002). 7 Birstein and Bemis (1997); EPIC (2001); Erickson et al. (2002). 8 Artyukhin and Andronov (1990). 9 Lelek (1987). 10 Zholdasova (1997). 11 Ong et al. (1996); Stabile et al. (1996); Smith and Clugston (1997); NMFS (1998b); Kynard and Horgan (2002); Waldman et al. (2002). 12 Krykhtin and Svirskii (1997). 13 Wei et al. (1997, 2004) 14 Rochard et al. (1990); Debus (1997); Williot et al. (1997). 15 Anders et al. (2002). 16 Birstein (1997b). 17 Salnikov et al. (1996). 18 Salnikov et al. (1996); Birstein (1997b). 19 Kallemeyn (1983); Mayden and Kuhajda (1996, 1997a); Campton et al. (2000); Bramblett and White (2001); Tranah et al. (2001). 20 Mayden and Kuhajda (1996); Keenlyne (1997); Campton et al. (2000); Bramblett and White (2001); Tranah et al. (2001). 21 Mayden and Kuhajda (1996, 1997b); Campton et al. (2000); Tranah et al. (2001). 22 Graham (1997); Jennings and Zigler (2000); Mims (2001). 23 Mims et al. (1993); Wei et al. (1997, 2004). Ó 2005 Blackwell Publishing Ltd, F I S H and F I S H E R I E S, 6,

6 Figure 1 Range and distribution of sturgeon and paddlefish populations. 1998; Doukakis et al. 1999). For example, molecular evidence suggests that the Persian sturgeon (A. persicus) may not be a separate species from the Russian sturgeon (A. gueldenstaedtii), although it is referred to as such herein as it is given distinct fisheries management attention (Berg 1934; Birstein and Bemis 1997; Birstein et al. 2000; Birstein and Doukakis 2002). Although life-history traits vary among species, Acipenseriformes are generally long-lived fishes that grow and mature slowly (Table 2; Fig. 2; Birstein 1993; Billard and Lecointre 2001). Most species are diadromous (migrating between marine and freshwater systems) and few are potamodromous (migrating within freshwater) with all species reproducing in freshwater, spawning in habitats with hard substrates (e.g. gravel, cobbles, boulders) of varying depths (from a few to over 20 m) and current velocities (e.g. from 0.5 to 2.2 m s )1 ) (Bemis and Kynard 1997; Billard and Lecointre 2001). The group exhibits one of the highest levels of polyploidy in fishes, ranging from 4n to 16n with chromosome numbers from 120 to 500 (Vasil ev 1999). It also includes the largest freshwater fish, the beluga sturgeon, Huso huso (Table 2). Nearly all Acipenseriformes are considered threatened or endangered because of the combined effects of overfishing and habitat degradation (Table 1; Rochard et al. 1990; Birstein 1993; De Meulenaer and Raymakers 1996; Billard and Lecointre 2001). Existing since the 5th century BC and referenced in ancient Greek, Roman and Chinese literature, sturgeon fisheries have intensified as gear and shipping technology has advanced and global demand for caviar increased (Birstein 1993; De Meulenaer and Raymakers 1996; Wei et al. 1997; Luk yanenko et al. 1999; Secor 2002). Mounting commercial pressure coincided with construction of river dams in Acipenseriformes habitat, blocking spawning ground access and altering spawning habitat, with fish passageways ineffective for mitigation and dam removal a limited option (Scarnecchia et al. 1989; NMFS 1998b; Dubina and Kozlitina 2000; Billard and Lecointre 2001; Friedl and Wüest 2002; Hart et al. 2002; Parsley et al. 2002; Secor et al. 2002). Pollution has also negatively affected reproduction, physiology and food availability as have introduced species, deforestation, water diversion, and gravel and sand extraction Shagaeva et al. 1993; Zaitsev 1993; Altuf ev 1997; Bacalbasa- Dobrovici 1997; Debus 1997; Ferguson and Duckworth 1997; Gorbunenko et al. 1997; Graham 1997; Krykhtin and Svirskii 1997; Ruban 1997; Bickham et al. 1998; Petr and 238 Ó 2005 Blackwell Publishing Ltd, FISH and FISHER IES, 6,

7 Table 2 Life history and catch statistics for commercial species. General references include Billard and Lecointre (2001) and Williamson (2003). Specific references noted below. Species L Max (M) W Max (kg) A Max (years) Historic/Current Peak catch (tonnes) Recent catch (tonnes) A. baerii ?/ (1930 s) 12 (2003) A. fulvescens > / (1885; Lake Erie); 223 (1997 Canada) A. gueldenstaedtii >50/38 > (early 1900s; Caspian) 399 (2003) (335 Caspian) A. medirostris ?/60?? A. o. oxyrinchus /? 3300 (1880; US); >200 (1880; CA) 73.6 (Canada) A. persicus /?? A. ruthenus /22? 6 (2003) A. schrenckii ?/ (1891) 45 (2003) A. stellatus / (1970s; Caspian) 305 (2003) (284.8 Caspian) A. transmontanus >100/ (1885; Sacramento-San Joaquin); 200 (2002) US 2500 (1892; Columbia); 512 (1897; Fraser) H. dauricus 6 > ?/ (1891) 88 (2003) H. huso 7 > / (early 1900 s; Caspian) (2003) (Caspian 155.4) S. platorynchus ?/30? 25 (1997) P. spathula ?/ (1899)? 1 Ruban (1997,1998); 2 EPIC (2001); in Erickson et al. (2002); 3 Smith and Clugston (1997); Gross et al. (2002); 4 Krykhtin and Svirskii (1997); Wei et al. (1997); Zhuang et al. (2002); 5 Parsley et al. (1993); Parsley and Beckman (1994); 6 Krykhtin and Svirskii (1997); 7 Raspopov (1993a,b); 8 Keenlyne (1997); Quist et al. (2002); Everett et al. (2003); 9 Carlson and Bonislawsky (1981); Epifano et al. (1996). 7 Spawning periodicity females (years) A. schrenckii A. brevirostrum P. spathula S. platorynchus S. suttkusi A. ruthenus S. albus H. dauricus A. medirostris A. fulvescens A. o. oxyrhinchus A. baerii A. gueldenstaedtii H. huso A. stellatus A. nudiventris A. o. destoi A. persicus A. transmontanus Age at maturity females (years) Figure 2 Sturgeon life-history traits; age at maturity and spawning periodicity for females. Values are midrange values of literature survey values. Note same point for H. dauricus and A. medirostris. Epifano et al. 1996; Krykhtin and Svirskii 1997; Ruban 1997, 1998; Mayden and Kuhajda 1997; Smith and Clugston 1997; Wei et al. 1997; Secor et al. 2000; Billard and Lecointre 2001; Erickson et al. 2002; Gross et al. 2002; Quist et al. 2002; Vecsei et al. 2002; Zhuang et al Mitrofanov 1998; Dubina and Kozlitina 2000; Jennings and Zigler 2000; Onders et al. 2001; Daskalov 2002; Friedl and Wüest 2002; Gucu 2002). Combined with late maturity and infrequent reproduction, overfished populations of low abundance have resulted. Ó 2005 Blackwell Publishing Ltd, F I S H and F I S H E R I E S, 6,

8 International harvest and trade Although commercial caviar trading has flourished globally, the geographical distribution of catch supplying trade has shifted through time. In the 19th century, the United States was the top caviar producer, exporting black caviar from the US waters (primarily from the Atlantic sturgeon A. oxyrinchus oxyrinchus) to Europe (Birstein 1997a; Secor 2002). By the early 1900s, US populations, production and export plummeted (De Meulenaer and Raymakers 1996; Hoover 1998). By the end of the 19th century, Russia was a major caviar trading nation and by the early 20th century Russian sturgeon harvests were seven times greater than historic peak US catches of Atlantic sturgeon (Taylor 1997; Secor et al. 2000). Commercial fisheries in Canada began in the late 19th century, but never commanded a substantial portion of the global market (Williamson 2003). Today, the Caspian Sea nations of Iran, Kazakhstan, Russia and to a lesser extent Azerbaijan and Turkmenistan, dominate the international trade in capture fisheries products while the US, Japan, the European Union and Switzerland are the major importers (De Meulenaer and Raymakers 1996; Hoover 1998; Raymakers 2002). Sturgeon and paddlefish fisheries catch is currently at its lowest in recent decades (Fig. 3). After peaking in the late 1970s, total global production (capture and aquaculture combined) fell, levelling off in the mid-1990s (Fig. 3). Capture fisheries have accounted for a decreasing percentage of overall production, with aquaculture production recently surpassing wild fisheries production (Fig. 3). In turn, the amount of caviar in international trade has dropped while the amount of meat from aquaculture has increased (Raymakers and Hoover 2002; Raymakers 2002). Aquaculture production of caviar, although increasing, has lagged behind meat production because of the time investment required for maturity and egg production. Trends in the production and trade in the last two decades have been tied to events in the Caspian Sea region, decreasing fisheries productivity, tightened international trade regulation, and aquaculture. The dissolution of the Soviet Union is considered to be a turning point in sturgeon fisheries management, after which increased illegal harvest and trade ensued, flooding the international market with illegal, low quality, inexpensive caviar (De Meulenaer and Raymakers 1996; Birstein 1997a; Taylor 1997; Vaisman and Raymakers 2001). Global imports of black caviar rose during the early-mid 1990s, with European imports increasing times and US imports increasing by 100% (De Meulenaer and Raymakers 1996; Birstein 1997a). Fraudulent mislabelling of caviar became problematic, with low value caviar and caviar from endangered species substituted for highly prized caviar (DeSalle and Birstein 1996; Birstein et al. 1998). Mounting concern about sturgeons and paddlefishes led to the 1997 listing of all species under the Convention on International Trade in Endangered Species (CITES), a voluntary international Total Capture Aquaculture Catch (thousand tonnes) Figure 3 World catch of sturgeon and paddlefish (Source: FISHSTAT Plus, Fisheries Data Analysis Software for Windows, FAO, Rome). Year 240 Ó 2005 Blackwell Publishing Ltd, FISH and FISHER IES, 6,

9 agreement between governments protecting species threatened by trade and the most significant international act protecting sturgeons and paddlefish. International trade in CITES protected species is accomplished through a trade permit system, for species threatened with extinction (Appendix I) and species of concern (Appendices II and III). Two species of Acipenseriformes are listed under Appendix I, with trade permitted only in special circumstances, and the remaining under Appendix II, with controlled trade permitted (Table 1). Given the challenges of Acipenseriformes conservation, the CITES parties have adopted a series of recommendations outlining conservation measures required for continued trade, including enhanced fishery management and legislation, regional coordination, labelling and control of illegal trade (Conf (rev); SC45 Doc.12.1, 12.2). Although implementation of these resolutions has been problematic, greater trade regulation and increased scrutiny of fisheries management have resulted. Legal and illegal trade in black caviar remains a lucrative business. Legal trade from Russia is estimated at $ million while the value of illegal Russian caviar exports has been estimated at $ million (Speer et al. 2000; Stone 2002). Black caviar can command up to US$ /kg for high quality beluga, with other wild and aquaculture caviar and roe commanding less (Table 3). Prices for both wild origin and aquaculture caviar have risen as wild origin caviar has Table 3 Caviar prices ($US, 2004) in internet survey. become scarcer and the taste and quality of aquaculture caviar has been improved, prompting greater acceptance in the marketplace (De Meulenaer and Raymakers 1996; Raymakers and Hoover 2002; Raymakers 2002). The international caviar trade remains dominated by product from the Caspian and Black Sea regions. Four Caspian/Black Sea species, beluga, stellate (A. stellatus), Russian and Persian, have supplied over 95% of the internationally traded caviar in recent years (2003: 94.8%; 2004: 99.6%). Other commercially important species include the Caspian Sea sterlet (A. ruthenus), Amur River sturgeon [kaluga sturgeon (H. dauricus), Amur sturgeon (A. schrenckii)], Siberian sturgeon (A. baerii), and North American species [white sturgeon (A. transmontanus), Atlantic sturgeon (A. oxyrinchus), lake sturgeon (A. fulvescens), American paddlefish (Polyodon spathula), shovelnose sturgeon (Scaphirhynchus platorynchus), and green sturgeon (A. medirostris)]. Species not commercially important and not discussed herein include A. mikadoi, A. naccarii, A. sturio, Yangtze River species (A. dabryanus, A. sinensis, P. gladius), Siberian populations of the sterlet, Aral Sea watershed species (A. nudiventris, P. kaufmanni, P. hermanni, P. fedtschenkoi), and US taxa listed under the US Endangered Species Act (ESA) (A. brevirostrum, S. albus, S. suttkusi, white sturgeon, Kootenai river, A. o. desotoi) (Table 1). Ship sturgeon (A. nudiventris) in the Caspian and Black Sea, although commercially exploited to a small extent and highly endangered, is not considered here because of the lack of data about the fishery (Table 1). Product name Species Price ($/oz) Price ($/kg) Major global fisheries Beluga Huso huso Osetra Acipenser gueldenstaedtii Sevruga A. stellatus White A. transmontanus Paddlefish Polyodon spathula Hackleback S. platorynchus Baerii A. baerii Persian A. persicus Salmon Whitefish Trout Bowfin Companies surveyed included Caviar direct, Caviar express, Caviar Russe, Marky s caviar, Mackenzie limited, Petrossian, Plaza de Caviar, The Golden Egg, and Tsar Nicoulai. Caspian Sea Fed by over 100 river systems, the Caspian Sea, at km 2, is the largest inland water body in the world and harbours the greatest abundance of sturgeon on the planet and largest and most important sturgeon fisheries (Figs 4 and 5; Dumont 1995; De Meulenaer and Raymakers 1996; Levin 1997; Secor et al. 2000). Six species of sturgeon occur in the basin [beluga, Russian, Persian, sterlet, stellate, ship (A. nudiventris)], with Russian and stellate sturgeons the most abundant and ship sturgeon the rarest (Levin 1997; CITES 2000). All species except sterlet (a potamodromous species) are anadromous, although landlocked freshwater Ó 2005 Blackwell Publishing Ltd, F I S H and F I S H E R I E S, 6,

10 Current Peak Black Sea/Danube Caspian Sea Sea of Azov Western Atlantic Lake Erie (lake) Columbia Ob River Mississippi R (paddlefish) Amur River Fraser River Yenisey River Lena River Production (thousand tonnes) Figure 4 Peak (right/higher value) and current (left/lower value) sturgeon fishery production by region. Figure 5 Caspian, Black and Sea of Azov regional map showing principal spawning rivers. Hatch marks indicate river dams. populations occur (Sokolov and Tsepkin 1996; Hensel and Holcik 1997; CITES 2000; Arai and Miyazaki 2001; Chebanov and Billard 2001). Anadromous species typically consist of autumnal and vernal (sometimes divided into early and late races), which migrate upriver in two separate seasonal runs, coincident with fishing seasons (Hensel and Holcik 1997; Levin 1997). All anadromous species but the Persian sturgeon, which occurs mainly in the southern Caspian region, are distributed throughout the Caspian Sea, while the freshwater sterlet primarily inhabits the Volga River (Berg 1948; Artyukhin and Zarkua 1986; Vlasenko et al. 1989; Artyukhin 1997). These species vary in life history, with all species but the sterlet requiring at least 10 years to mature (Table 2; Fig. 2). Historically the Volga River has been the most important river for the fishery and for spawning but dam construction on the Volga River has deprived sturgeons of between 30% and 90% of their former 242 Ó 2005 Blackwell Publishing Ltd, FISH and FISHER IES, 6,

11 spawning grounds (Fig. 5; De Meulenaer and Raymakers 1996; Khodorevskaya et al. 1997; Secor et al. 2000). Currently the Ural River is the only free-flowing river feeding the Caspian Sea where sturgeons reproduce unhindered by dams, although sedimentation and pollution have caused a 50% loss in spawning area (De Meulenaer and Raymakers 1996; Khodorevskaya et al. 1997; in Secor et al. 2000). The Gorganrug, Kura, Sefidrud, Sulak, Tajen and Terek rivers may also provide sturgeon habitat (Khodorevskaya et al. 1997; CITES 2000). After hatching in river systems, anadromous sturgeons migrate into the sea to mature, returning to river systems for spawning, with homing fidelity to natal rivers uncertain (Khodorevskaya and Krasikov 1999; Khodorevskaya et al. 2000; Billard and Lecointre 2001; Kynard et al. 2002). The northern Caspian Sea (specifically the Volga River) historically supported the bulk of the sturgeon catch with southern Caspian Sea catch increasing in recent years (De Meulenaer and Raymakers 1996; Artyukhin 1997; Khodorevskaya et al. 1997). Catch in the Caspian Sea peaked in the 17th century ( tonnes) followed by declines and rebounds due to reduced effort coincident with wars (e.g ) and fisheries regulation. In the 20th century, catch peaked in the 1970s ( tonnes), but declined steadily thereafter to 1388 tonnes in 2002 (Fig. 4; FISHSTAT; De Meulenaer and Raymakers 1996; Artyukhin 1997; Birstein 1997a; Levin 1997; Khodorevskaya et al. 2000; Secor et al. 2000; Vaisman and Raymakers 2001). Caspian Sea catch is comprised of Russian, stellate, and Persian sturgeon and to a lesser extent, beluga and sterlet (Artyukhin 1997; Khodorevskaya and Krasikov 1999; Moghim and Neilson 1999). Beluga catch has steadily declined from a peak in the early 1900s ( tonnes) while catch of Russian sturgeon has been more variable, also exhibiting an overall decline (Table 2; Fig. 6a,b). Fewer data on the stellate sturgeon fishery are available with catch declines evident from 1970 to 2002 (Table 2; Fig. 6c). Although historic data on Persian and sterlet sturgeon are scarce, Persian sturgeon catch has risen in recent years while sterlet catch has never been significant (Table 2). Published studies illustrate that population sizes of all species but Persian sturgeon have declined, with some estimates suggesting 80 90% decreases in the last years (Khodorevskaya and Krasikov 1999; Khodorevskaya et al. 2002). The number of beluga sturgeon annually entering the Volga to spawn dropped from during to 2800 during , while only 2500 individuals migrated up the Ural River in 2002 (Khodorevskaya et al. 1997, 2000; J. A. Armstrong, unpublished data). For beluga, Russian, stellate and sterlet sturgeon, size at maturity, growth rate and average age of the population and of spawning individuals have decreased (Raspopov 1993a,b; Khodorevskaya et al. 1995, 1997, 2000, 2002; Khodorevskaya and Krasikov 1999; Khodorevskaya 1999; Moghim and Neilson 1999; Kuznetsov 2000). Sex ratios have shifted, with some populations consisting of fewer than 20% females (Khodorevskaya 1999; in De Meulenaer and Raymakers 1996; Vaisman and Raymakers 2001). In contrast, abundance estimates generated through sea trawl studies conducted by range states in compliance with CITES resolutions suggest large population sizes and increasing abundance. Independent review of the studies could not replicate the findings, suggesting erroneous calculations overestimating abundance (Pikitch and Lauck, unpublished data in Pearce 2003). Alternative calculations indicate dangerously small populations of beluga and harvest quotas equivalent to removal of nearly all mature individuals (Pikitch and Lauck unpublished data; Ginsberg 2002). Current, accepted population assessments are still unavailable. The Caspian Sea fishery was reportedly tightly regulated in Soviet times, with fishing banned in the open sea, catch quotas, seasonal closures and gear restrictions (De Meulenaer and Raymakers 1996; Birstein 1997a; Levin 1997; Taylor 1997; Khodorevskaya et al. 2000; Secor et al. 2000). The dissolution of the Soviet Union in 1991 led to the division of fishing rights among the new independent states, sea fishing, and increased illegal harvest and trade (De Meulenaer and Raymakers 1996; Levin 1997; Taylor 1997). In 1997, the Caspian nations re-instituted the sea fishing ban, allowing harvest only in rivers, but the ban is not adequately enforced (Bauer 1997). Fisheries are now managed and regulated by individual countries through gear, catch and seasonal restrictions, with exports managed under CITES (De Meulenaer and Raymakers 1996; CITES 2000; Khodorevskaya et al. 2000; Vaisman and Raymakers 2001). Recommendations set forth after a CITES Review of Significant Trade (A CITES action when Appendix II species are thought to be traded without adequate implementation of CITES provisions. Beluga, Persian, Russian, ship, sterlet, and Ó 2005 Blackwell Publishing Ltd, F I S H and F I S H E R I E S, 6,

12 (a) Catch (thousand tonnes) (c) Catch (thousand tonnes) Year Year (b) Catch (thousand tonnes) (d) Catch (thousand tonnes) Year Year (e) Catch (thousand tonnes) Year (f) Catch (thousand tonnes) Year (g) Catch (thousand tonnes) Year (h) Catch (thousand tonnes) Year Figure 6 Catch data over time for select species. (a) Beluga (Caspian Sea) (Raspopov 1993a; in Khodorevskaya et al. 1997, 2000; CITES 2000; Altukhov and Evsyukov 2001; (b) Russian sturgeon (Caspian Sea) (De Meulenaer and Raymakers 1996; Khodorevskaya et al. 1997; CITES 2000; Altukhov and Evsyukov 2001; (c) Stellate sturgeon (Caspian Sea) (Khodorevskaya et al. 1997; CITES 2000; Altukhov and Evsyukov 2001; (d) Siberian sturgeon (Ob, Yenisey, Lena Rivers) (Ruban 1997; CITES 2000); (e) white sturgeon (Columbia River) (Rieman and Beamesderfer 1990; Parsley and Beckman 1994; Williamson 2003); (f) green sturgeon (EPIC 2001). (g) Atlantic sturgeon (US landings only until fishery closure) (Smith and Clugston 1997; Atlantic Sturgeon Status Review Team 1998; Waldman and Wirgin 1998; Secor 2002); (h) Paddlefish (Commercial harvest only) (Carlson and Bonislawsky 1981; CITES 2000). Note different scales for each graph. stellate, sturgeon were reviewed) called on Caspian nations to establish coordinated basin-wide management, long-term, comprehensive stock surveys, measures to combat illegal harvest and improve fishery management (SC45 Doc.12.2; Conf. 12.7). Export quotas were to be based on a cooperative management strategy, agreed upon by all Caspian nations, and submitted to the CITES Secretariat for review by December 31 of the year preceding export. Since 2001, approved quotas have been reduced for all species but Persian sturgeon (Table 4, Fig. 7). Problems with CITES compliance has resulted in temporary fishery closures, trade bans and zero quotas, but long-term bans have never been instituted despite the fact that many recommendations remain outstanding (Raymakers 2002; Raymakers 244 Ó 2005 Blackwell Publishing Ltd, FISH and FISHER IES, 6,

13 (a) (b) Beluga Stellate Persian Russian Beluga Stellate Persian Russian Figure 7 Evolution of CITES export quotas for four main commercial species (a) Meat; (b) caviar. and Hoover 2002; Stone 2002; Ginsberg 2002). Critics believe enforcement of resolutions has been weak and fishery collapse and/or extinction may be imminent. Illegal harvest still exceeds legal catch by several orders of magnitude and recent news suggests most black caviar in trade is illegal (Vaisman and Raymakers 2001; Agence France Presse 2004; ITAR-TASS News Agency 2004). Domestic caviar sale and consumption in Caspian range countries has reportedly increased since CITES listing, making it questionable as to whether export restrictions have resulted in decreased harvest (Vaisman and Raymakers 2001; Raymakers and Hoover 2002). Export quotas are still being approved in the absence of accepted population abundance estimates. In the 1950s, captive propagation programmes (whereby sturgeons are bred in captivity for restocking wild populations) were created to ameliorate population declines and the loss of natural recruitment (Levin 1997; CITES 2000; Secor et al. 2000). In the early 1990s, million individuals were released from hatcheries annually, including beluga, Persian, Russian, ship, stellate and sterlet (Levin 1997; CITES AC 18 Doc ). It is speculated that 30% (Volga River stellate and Russian sturgeon) to 90% (Volga River beluga) of wild individuals are of hatchery origin (De Meulenaer and Raymakers 1996; Khodorevskaya 1999; Khodorevskaya et al. 2000; Secor et al. 2000). As released fish have not been tagged or marked, estimating their contribution to the current population is impossible, although some programmes are beginning to address this issue (Doukakis et al. 2004). Hatchery programmes have been faltering in recent years because of inadequate financing and a scarcity of breeding females (Khodorevskaya 1999; Khodorevskaya et al. 2000; Secor et al. 2000; Doukakis et al. 2004). Black Sea and Sea of Azov The Black Sea, Sea of Azov, and their watersheds once harboured some of the most productive sturgeon fisheries (Figs 4 and 5; Birstein 1996; Vaisman and Raymakers 2001). The six species found in the Caspian Sea inhabit these basins and the Baltic sturgeon, A. sturio, formerly occurred in the Black Sea, but has been extirpated (Hensel and Holcik 1997). The region now contributes little to international trade, with 6.5 tonnes of caviar and 50 tonnes of meat (5% and 13% of total export, respectively) exported in 2004 from the Black Sea (Table 4). Beluga and ship sturgeons are scarce or extinct in the Sea of Azov, with the last records of beluga from the mid 1980s (in Khodorevskaya 1999; CITES 2000; Billard and Lecointre 2001). Sterlet is plentiful in the Danube and Dneister rivers, but its status in the Sea of Azov is uncertain (Bacalbasa-Dobrovici 1997; Hensel and Holcik 1997; CITES 2000). Persian sturgeon, with populations in Georgia (Rioni River), Russia (Don River), and Turkey, have experienced a 50% decline in the last three generations (AC 18 Doc ). As in the Caspian, dams have practically eliminated natural reproduction of populations in the upper and middle Danube River, and in the Dneister River and the Don and Kuban rivers of the Sea of Azov (Fig. 5; Bacalbasa-Dobrovici 1997; Gorbunenko et al. 1997; Hensel and Holcik 1997; CITES 2000; Billard and Lecointre 2001; Dubina and Kozlitina 2000; Friedl and Wüest 2002). Although sturgeons historically reproduced in many Black Sea river systems, only the Danube River currently supports significant spawning populations (Fig. 5; Bacalbasa-Dobrovici 1997; Hensel and Holcik 1997; CITES 2000). Stellate, beluga and Ó 2005 Blackwell Publishing Ltd, F I S H and F I S H E R I E S, 6,

14 Table 4 CITES export quotas for meat (M) and caviar (C). Species Country/ Region 2001 (M) 2002 (M) 2003 (M/FC) 2004 (M/FC) 2005 (M/FC) Trend (M) 2001 (C) 2002 (C) 2003 (C) 2004 (C) 2005 (C) Trend (C) A. gueldenstaedtii Azov fl fl Black F fl Caspian F fl Total F fl A. persicus Caspian F F A. ruthenus Black Caspian « «Total A. stellatus Azov fl fl Black fl fl Caspian F fl Total F fl H. huso Black F fl Caspian fl fl Total fl fl A. schrenckii China Ip « Ip «Russia Ip fl Ip fl Total Ip fl Ip fl H. dauricus China Ip « Ip «Russia Ip fl Ip fl Total Ip fl Ip fl A. fulvescens Canada fl fl A. o. oxyrinchus Canada fl fl A. transmontanus US fl fl Export quotas were not issued for wild products from A. baerii, A. medirostris, S. platorynchus or P. spathula during this period. Trend arrows display increasing ( ), decreasing (fl), steady («) or fluctuating trends (F) in export quotas. FC, Food and Canned Products; Ip, discussions in progress for issuing quota. Russian sturgeon have been extirpated from the upper Danube (source-vienna), are critically endangered or rare in the middle portion of the river (Vienna-Iron Gates Dam I), and are vulnerable in the lower river (Iron Gates Dam I-mouth) (Fig. 5; Bacalbasa-Dobrovici 1997; Hensel and Holcik 1997). Sterlet occurs in the middle and lower reaches and rarely in the upper Danube (Bacalbasa- Dobrovici 1997; Hensel and Holcik 1997). Ship sturgeon is critically endangered throughout the Danube basin, existing only as a freshwater form (Hensel and Holcik 1997). Other important rivers include the Bug, Coruh, Dnieper, Dniester, Inguri, Kizilirmak, Lenkoranka, Rioni, Supsa, Tisza and Yesilirmak in the Black Sea, and the Don and Kuban rivers in the Sea of Azov although it is unlikely that natural reproduction continues in the Sea of Azov. Catch in the Black Sea watershed is conducted by Romania, Ukraine, Bulgaria and Serbia. Historic catch records, available mostly for the Danube River, indicate declines in the Danube River fishery as early as the 19th century, continuing through the 1960s (300 tonnes; 1960) the middle 1990s (9.4 tonnes; 1995) (Bacalbasa-Dobrovici 1997). Catch of Russian sturgeon has fluctuated, from 25 tonnes annually in the Danube from 1958 to 1981 to 11 tonnes in 1999 to 19 tonnes in 2003 (Table 2; CITES 2000). Beluga sturgeon declines in the Danube River were reported beginning in the 16th century, with recent catches below 60 tonnes (Hensel and Holcik 1997). Stellate catch has always been small while sterlet catch has been higher, dominated by Bulgaria and export accomplished by Romania (Table 4; CITES 2000). Published abundance estimates are not available for Black Sea populations but an increasing proportion of immature animals was observed in stellate populations in the Danube River (Ceapa et al. 2002). In the Sea of Azov legal fishing by Russia and Ukraine has practically ceased and no export quotas have been issued for the last 2 years (Table 4). Peak catch from the 1930s to 1962 was 7000 tonnes, declining to 1103 tonnes in the early 1960s to 200 tonnes by 1998 to 70 tonnes in 2003, 246 Ó 2005 Blackwell Publishing Ltd, FISH and FISHER IES, 6,

15 dropping up to 90% in some regions between 1993 and 1998 (Vaisman and Raymakers 2001). In the mid-1980s, the biomass of stellate and beluga sturgeon in the Sea of Azov was tonnes and tonnes, respectively, before pollution related die-offs that began in 1990 (Volovik et al in CITES 2000). Biomass estimates for Russian sturgeon are only available for 1993 and are lower than stellate and beluga (44.8 tonnes) (CITES 2000). Fisheries regulations in the Black Sea [Bulgaria, Romania, Serbia and Ukraine (Russian sturgeon only)] are determined by individual countries including breeding season closures, gear restriction and minimum size requirements (CITES 2000). Black Sea and Sea of Azov nations communicate export quotas to the CITES Secretariat for approval and Black Sea nations have formed a regional management group (Black Sea Sturgeon Management Group) in fulfilment of CITES recommendations. CITES export quotas have been reduced since 2001, with the exception of sterlet quotas (Table 4). Illegal fishing is still problematic in both the Black Sea and the Sea of Azov, where illegal catch is estimated to be times higher than the legal catch (Bacalbasa-Dobrovici 1997; in CITES 2000; Navodaru et al. 2001; Vaisman and Raymakers 2001). Captive propagation and release is employed in the Black Sea and Sea of Azov (CITES 2000; Chebanov and Billard 2001; in Smith et al. 2002a). The Sea of Azov formerly had seven hatcheries releasing 39 million juveniles annually (7% beluga, 43% Russian, 49% stellate), but many hatcheries are not functioning because of financial constraints and lack of broodstock (in Birstein 1997a; Vaisman and Raymakers 2001). Over 30 million individuals were released into the Don and Kuban rivers in 1999 and 2000 (Chebanov et al. 2002). Up to 100% of beluga sturgeon in the Sea of Azov are allegedly derived from hatcheries, compared with 80 to 95% of Russian and 60 98% of stellate sturgeon (CITES 2000). Without tagging and monitoring programmes it is impossible to verify stocking success. Amur River basin The 4000 km Amur River basin forms the border between Russia and China for one-third of its length and harbours two endemic commercially exploited sturgeons, the kaluga and Amur sturgeon (Fig. 1; Krykhtin and Svirskii 1997; Wei et al. 1997). Kaluga is a large, long-lived, late maturing, predominantly freshwater species while the Amur sturgeon is a smaller, strictly freshwater species maturing earlier than kaluga (Table 2; Fig. 2). Caviar produced from these species is referred to as kaluga (kaluga sturgeon) and osietra (Amur sturgeon). Sturgeon catch in the Amur River peaked in 1891 (1195 tonnes; Table 2). In the last century, catch fluctuated between 100 tonnes to 400 tonnes annually on the Chinese side of the river and since the 1990s has been below 100 tonnes on the Russian side (Krykhtin and Svirskii 1997; Wei et al. 1997; CITES 2000; Zhuang et al. 2002). In 2003, 205 tonnes (120 tonnes China and 85 tonnes Russia) was caught overall, with 67 tonnes of Amur sturgeon and 138 tonnes of kaluga. Export quotas for both species have decreased since 2001 (Table 4). As of 1997, population estimates for the four distinct populations of kaluga were as follows, with relatively few mature fish in any population: estuary (70 000), lower (40 000) and middle (30 000), upper Amur River (unavailable) (Krykhtin and Svirskii 1997). For Amur sturgeon, population estimates from the 1990s indicate about 3000 individuals in the estuarine populations, in the lower Amur, and in the middle Amur. Limits on catch in the 1970s resulted in population increases, but decreases, especially in the number of mature individuals, followed, in part, because of an illegal fishery in the lower Amur River (Krykhtin and Svirskii 1997). Catch records from the Chinese side of the Amur River indicate declines in both species, but accurate assessments are needed (Wei et al. 2004). China and Russia manage Amur River populations under national regulations with export under CITES. Fishing for Amur sturgeon in China is regulated by gear, size limits, licensing, season and area (Wei et al. 1997, 2004; CITES 2000). Amur sturgeon fisheries have been banned in Russia since 1958 with catch for scientific purposes only, although Russia reportedly exceeds the scientific quota (Krykhtin and Svirskii 1997; CITES 2000). Implementation of regulations and illegal fishing are problematic and better joint management between Russia and China has been recommended (Krykhtin and Svirskii 1997; Wei et al. 1997, 2004; CITES 2000). Since 2001, CITES export quotas for kaluga and Amur sturgeon have decreased or remained constant (Table 4). Ó 2005 Blackwell Publishing Ltd, F I S H and F I S H E R I E S, 6,